International Journal of Primatology

, Volume 29, Issue 5, pp 1341–1353

Mitochondrial COII Introgression into the Nuclear Genome of Gorilla gorilla

Article

Abstract

Numts are nonfunctional mitochondrial sequences that have translocated into nuclear DNA, where they evolve independently from the original mitochondrial DNA (mtDNA) sequence. Numts can be unintentionally amplified in addition to authentic mtDNA, complicating both the analysis and interpretation of mtDNA-based studies. Amplification of numts creates particular issues for studies on the noncoding, hypervariable 1 mtDNA region of gorillas. We provide data on putative numt sequences of the coding mitochondrial gene cytochrome oxidase subunit II (COII). Via polymerase chain reaction (PCR) and cloning, we obtained COII sequences for gorilla, orangutan, and human high-quality DNA and also from a gorilla fecal DNA sample. Both gorilla and orangutan samples yielded putative numt sequences. Phylogenetically more anciently transferred numts were amplified with a greater incidence from the gorilla fecal DNA sample than from the high-quality gorilla sample. Data on phylogenetically more recently transferred numts are equivocal. We further demonstrate the need for additional investigations into the use of mtDNA markers for noninvasively collected samples from gorillas and other primates.

Keywords

gorilla mtDNA noninvasive samples numts 

References

  1. Anthony, N. M., Clifford, S. L., Bawe-Johnson, M., Abernethy, K. A., Bruford, M. W., & Wickings, E. J. (2007). Distinguishing gorilla mitochondrial sequences from nuclear integrations and PCR recombinants: Guidelines for their diagnosis in complex sequence databases. Molecular Phylogenetics and Evolution, 43, 553–566. doi:10.1016/j.ympev.2006.09.013.PubMedCrossRefGoogle Scholar
  2. Bensasson, D., Zhang, D., Hartl, D. L., & Hewitt, G. M. (2001). Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends in Ecology & Evolution, 16, 314–321. doi:10.1016/S0169-5347(01)02151-6.CrossRefGoogle Scholar
  3. Clifford, S. L., Anthony, N. M., Bawe-Johnson, M., Abernethy, K. A., Tutin, C. E., White, L. J., et al. (2004). Mitochondrial DNA phylogeography of western lowland gorillas (Gorilla gorilla gorilla). Molecular Ecology, 13, 1551–1565, 1567. doi:10.1111/j.1365-294X.2004.02140.x.PubMedCrossRefGoogle Scholar
  4. Collura, R. V., & Stewart, C. B. (1995). Insertions and duplications of mtDNA in the nuclear genomes of Old World monkeys and hominoids. Nature, 378, 485–489. doi:10.1038/378485a0.PubMedCrossRefGoogle Scholar
  5. Greenwood, A. D., & Pääbo, S. (1999). Nuclear insertion sequences of mitochondrial DNA predominate in hair but not in blood of elephants. Molecular Ecology, 8, 133–137. doi:10.1046/j.1365-294X.1999.00507.x.PubMedCrossRefGoogle Scholar
  6. Hasegawa, M., Kishino, H., & Yano, T. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22, 160–174. doi:10.1007/BF02101694.PubMedCrossRefGoogle Scholar
  7. Hazkani-Covo, E., & Graur, D. (2007). A comparative analysis of numt evolution in human and chimpanzee. Molecular Biology and Evolution, 24, 13–18. doi:10.1093/molbev/msl149.PubMedCrossRefGoogle Scholar
  8. Jensen-Seaman, M. I., Sarmiento, E. E., Deinard, A. S., & Kidd, K. K. (2004). Nuclear integrations of mitochondrial DNA in gorillas. American Journal of Primatology, 63, 139–147. doi:10.1002/ajp.20047.PubMedCrossRefGoogle Scholar
  9. Mundy, N. I., Pissinatti, A., & Woodruff, D. S. (2000). Multiple nuclear insertions of mitochondrial cytochrome b sequences in callitrichine primates. Molecular Biology and Evolution, 17, 1075–1080.PubMedGoogle Scholar
  10. Ruvolo, M., Disotell, T. R., Allard, M. W., Brown, W. M., & Honeycutt, R. L. (1991). Resolution of the African hominoid trichotomy by use of a mitochondrial gene sequence. Proceedings of the National Academy of Sciences of the United States of America, 88, 1570–1574. doi:10.1073/pnas.88.4.1570.PubMedCrossRefGoogle Scholar
  11. Ruvolo, M., Pan, D., Zehr, S., Goldberg, T., Disotell, T. R., & von Dornum, M. (1994). Gene trees and hominoid phylogeny. Proceedings of the National Academy of Sciences of the United States of America, 91, 8900–8904. doi:10.1073/pnas.91.19.8900.PubMedCrossRefGoogle Scholar
  12. Ruvolo, M., Zehr, S., von Dornum, M., Pan, D., Chang, B., & Lin, J. (1993). Mitochondrial COII sequences and modern human origins. Molecular Biology and Evolution, 10, 1115–1135.PubMedGoogle Scholar
  13. Saitou, N., & Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.PubMedGoogle Scholar
  14. Schmitz, J., Piskurek, O., & Zischler, H. (2005). Forty million years of independent evolution: a mitochondrial gene and its corresponding nuclear pseudogene in primates. Journal of Molecular Evolution, 61, 1–11. doi:10.1007/s00239-004-0293-3.PubMedCrossRefGoogle Scholar
  15. Swofford, D. L. (2001). PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Mehtods). Version 4. Sunderland, MA: Sinauer Associates.Google Scholar
  16. Thalmann, O., Hebler, J., Poinar, H. N., Pääbo, S., & Vigilant, L. (2004). Unreliable mtDNA data due to nuclear insertions: A cautionary tale from analysis of humans and other great apes. Molecular Ecology, 13, 321–335. doi:10.1046/j.1365-294X.2003.02070.x.PubMedCrossRefGoogle Scholar
  17. Thalmann, O., Serre, D., Hofreiter, M., Lukas, D., Eriksson, J., & Vigilant, L. (2005). Nuclear insertions help and hinder inference of the evolutionary history of gorilla mtDNA. Molecular Ecology, 14, 179–188. doi:10.1111/j.1365-294X.2004.02382.x.PubMedCrossRefGoogle Scholar
  18. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–4882. doi:10.1093/nar/25.24.4876.PubMedCrossRefGoogle Scholar
  19. Zischler, H., Geisert, H., & Castresana, J. (1998). A hominoid-specific nuclear insertion of the mitochondrial D-loop: Implications for reconstructing ancestral mitochondrial sequences. Molecular Biology and Evolution, 15, 463–469.PubMedGoogle Scholar
  20. Zischler, H., Geisert, H., von Haeseler, A., & Pääbo, S. (1995). A nuclear ‘fossil’ of the mitochondrial D-loop and the origin of modern humans. Nature, 378, 489–492. doi:10.1038/378489a0.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Department of AnthropologyHunter College of the City University of New YorkNew YorkUSA
  2. 2.Department of AnthropologyPrograms in Anthropology and Biology, The Graduate Center of the City University of New YorkNew YorkUSA
  3. 3.Department of Biological SciencesNorthern Arizona UniversityFlagstaffUSA

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